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Avian Adrenal Medulla: Cytomorphology and Function

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Avian Adrenal Medulla: Cytomorphology and Function View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Publications of the IAS Fellows Volume 45(1-4):1-11, 2001 Acta Biologica Szegediensis http://www.sci.u-szeged.hu/ABS REVIEW ARTICLE Avian adrenal medulla: cytomorphology and function Asok Ghosh, Stephen W. Carmichael1*, Monisha Mukherjee Department of Zoology, University of Calcutta, Calcutta, India, 1Department of Anatomy, Mayo Clinic/Foundation, Rochester, Minnesota, USA ABSTRACT The purpose of this review is to explore the world literature on the avian adrenal KEY WORDS medulla from the last 20 years. Unlike the mammalian adrenal medulla, the adrenal gland in adrenal medulla birds has chromaffin cells mixed with cortical cells. Studies have investigated the ultrastructure birds (both transmission and scanning electron microscopy), biochemistry, and physiology (partic- morphology ularly interactions with other endocrine glands) of the avian adrenal medulla. Although function progress has been made, it is apparent that research on the avian adrenal medulla still lags behind work on the mammalian organ. Acta Biol Szeged 45(1-4):1-11 (2001) The adrenal glands of birds, like those in mammals, are in the adrenal medulla. This profound variation of medullary paired yellow- or orange-colored pear- or triangle-shaped E/NE ratio in birds suggests a distinct evolutionary pattern glands that are next to the kidneys. The intermingling nature (Ghosh 1977, 1980). The avian phylogeny used in this study of cortical and medullary components constitutes a major was essentially based on palaeontological evidences (Grego- characteristic of avian adrenal medulla (Vestergaard and ry 1957). We feel that our “claim” of hormonal taxonomy is Willeberg 1978). This is in sharp contrast with its mammalian to be re-examined in view of cladistic (Cracraft 1988) and counterpart, where the medulla always occupies the central molecular (Mindell 1997) analyses of avian taxa (also portion and remains encircled by the adrenal cortex with its Bhattacharyya, B. 1999, personal communication). Later three concentric zones. Mahata and Ghosh (1986a, c, 1988) reported that NE and E Compared to the adrenal cortex, the avian adrenal medul- contents vary not only between birds of different phylogene- la was a much-neglected subject until the 1950s. Ghosh (This tic groups, but also with the age of birds of the same species. will refer to Asok Ghosh. His son, also an active scientist in the field, will be referred to as Subho Ghosh) and his I. Morphological considerations collaborators pioneered efforts to elucidate various aspects A. Development of avian endocrinology, particularly the adrenal gland (Ghosh 1977). This first review article on this subject was published Elegant work from Unsicker’s laboratory (Ross et al. 1995) by Ghosh, that covered works up to 1977. Later, a second shows that by embryonic day 15 (E15) sympathetic ganglia review by Ghosh in 1980 gave literature coverage from 1978 of chick embryos contain a glucocorticoid-responsive pro- to 1980. The present article will emphasize the world’s genitor population that can differentiate into medullary cells. literature on the avian adrenal medulla from 1981 through Another important work by Sanchez-Montesinos et al. (1996) 2000. examined the development of the chick sympathoadrenal Ghosh and his collaborators (see Ghosh 1977, 1980) system by identifying antibodies that recognized signal studied the relative proportion of epinephrine (E)- and molecules. Three expression patterns were found in the norepinephrine (NE)-secreting cells and cellular areas in the developing adrenal gland defining early permanent markers adrenal medulla of a number of birds representing several (chromogranins A and B, GaO, TH, and galanin); others orders and families. The data shows extreme variation in the (DbH, somatostatin, enkephalin, secretogranin 11, NPY, and relative concentration of E and NE cells in avian adrenal PNMT) follow as development proceeds. medulla that is not seen in other vertebrate groups. Light and ultrastructural studies (Subho Ghosh 1977) revealed that the B. Subcellular morphology orders with a more primitive ancestry contain more NE cells, During the last three decades, the cytophysiology of the avian whereas the more recently evolved birds possess more E cells adrenal medulla has been thoroughly worked out by Ghosh and his associates by means of histological, histochemical Accepted May 18, 2001 (Ghosh 1980), transmission (TEM; Ghosh et al. 1996a), and *Corresponding author. E-mail: [email protected] scanning (SEM; Guha et al. 1990) techniques. 1 Avian adrenal medulla: cytomorphology and function Maitra and Ghosh (1980) differentiated the two types of on woodpecker, kingfisher, parakeet, and common snipe tinctorially different adrenomedullary cells in the plum- (Guha et al. 1990). The presence of blebs, cords, globules, headed parakeet (Psittacula cyanocephala) by application of granular particulates, filamentous, and coral-like aggregates a modification of the Wood (1963) technique. The E cell on the adrenal surfaces also show great inter-specific varia- islets become densely granulated and reddish-brown colored, tions. In the rose-ringed parakeet, SEM observations reveal whereas the NE cells are homogeneously yellowish in color, densely granulated medullary cells, and a cytoplasm con- smaller in size, and fewer in number. The E- and NE- taining a single central or eccentric nucleus. Prominent secreting cells are also different on the basis of their mor- microvillus-like projections are seen that appear to connect phology, size, opacity, and fine structure of the vesicles (see nucleus with surrounding cytoplasm. The vesicles are oval, Unsicker 1973a, b, c; Ghosh and Guha 1988). round, or cylindrical and are frequently seen to fuse with one Unsicker (1973a, b, c) reported that E and NE cells could another. Also there occurs conglomeration of bleb-like be distinguished from each other on the basis of their structures in the blood spaces. The endothelium has rufflings structure and granulations. E cells exist in all avians, but in and breakages at points from which blebs appear to be corvids (includes crows, ravens, rooks, magpies, and jack- discharged (Carmichael et al. 1983). daws) and in some passers, they possess low electron dense vesicles and lack complete membranes. The average size of C. Immunocytochemistry NE vesicles in domestic chicken (Gallus domesticus) is By immunocytochemistry, it is suggested by Ohmori et al. greater (224 nm) than the E (168 nm) vesicles (Coupland (1997) and Ohmori (1998) that serotonin, galanin, chole- 1971). The E and NE vesicles follow a similar pattern in the cystokinin, met-enkephalin, somatostatin, and natriuretic rose-ringed parakeet (Psittacula krameri; Carmichael et al. polypeptides exist in chicken chromaffin cells, in addition to 1983) and in duck and geese (Guzsal and Hassan 1975). In E and NE. Different biogenic amines and neuropeptides the migratory snipe (Capella gallinago), only NE types of localized in medullary cells may regulate corticosterone chromaffin cells are observed (Carmichael et al. 1985). In secretion from interrenal cells via a paracrine mode of pigeons (Columba livia) and bulbuls (Pycnonotus cafer), two communication (cf. Nussdorfer 1996). distinct cell types are present. Although the vesicles of cells in pigeons do not manifest size difference, in bulbuls the E II. Biochemical aspects vesicles are comparatively large (Ghosh and Guha 1988). Cuello (1970) found a wide range of sizes of NE vesicles (80- A. Biosynthesis 500 nm) in the gentoo penguin (Pygoscelis papua). The TEM Aspects of biosyntheses have been discussed earlier (Ghosh studies by Guzsal and Hassan (1975) reveal presence of the 1977, 1980). The dopamine antagonist haloperidol stimulates so-called “dark cells” and the transitory sympathicoblasts in aldosterone and corticosterone secretion in rats (Goebel et al. the adrenal medulla of ducks and geese. 1992) and inhibits specific high affinity binding sites in the TEM studies of adrenal gland enables differentiation of membrane of adrenal medulla (Rogers et al. 1989). Recent the E and NE cells by their morphology, size, opacity, and work in rats by Mukherjee et al. (1995) shows significant fine structure of the vesicles (vide supra). But, in contrast to release of corticosterone following haloperidol treatment. the mammalian adrenal medulla, it has not been resolved The catecholamine content of adrenal medulla remains non- whether E and NE cells originate from the same, or two responsive, probably due to the specific blocking of the D2- separate cell types, of the adrenal medulla (Ghosh and Guha dopamine receptors. This aspect has remained unresolved in 1988). Recently, an electron microscopic study of the chro- avians and needs intense attention. maffin cells in the adrenal gland of 13 species of birds from Studies on rats show that the enzyme phenylethanolamine the Indian subcontinent was performed by Subho Ghosh et N-methyltransferase (PNMT) is localized in the E cells only. al. (1996a). The study revealed that the cytoarchitecture of Using an immunocytochemical technique, our laboratory the adrenal medulla is similar in many respects in all the group (Guha et al. 1992) indicates that PNMT location is birds. However, differences were noted in the density of similar at least among phylogenetically close avian species. chromaffin vesicles, subunit organization in certain vesicles, Unlike mammals, no particular cell specificity for
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